HAL Id: hal-00891945
https://hal.archives-ouvertes.fr/hal-00891945
Submitted on 1 Jan 2008
HAL is a multi-disciplinary open access
archive for the deposit and dissemination of
sci-entific research documents, whether they are
pub-lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.
L’archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d’enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.
The biology of a Patellapis (s. str.) species
(Hymenoptera: Apoidea: Halictidae): sociality
described for the first time in this bee genus
Kim Timmermann, Michael Kuhlmann
To cite this version:
Original article
The biology of a Patellapis (s. str.) species (Hymenoptera:
Apoidea: Halictidae): sociality described for the first time
in this bee genus*
Kim T
immermann
, Michael K
uhlmann
Institute of Landscape Ecology, University of Münster, Robert-Koch-Str. 26, 48149 Münster, Germany Received 3 July 2007 – Revised 12 October 2007 – Accepted 30 October 2007
Abstract – The sweat bees are socially diverse and therefore make ideal subjects for the study of insect sociality. A small nest aggregation of an undescribed species of Patellapis (s. str.) was studied in the western South African winter rainfall area to provide information on nest architecture, floral hosts, seasonality and kleptoparasites. A single excavated nest was inhabited by eight females and consisted of a main burrow with several lateral tunnels. Observations indicate that this Patellapis species probably has a communal nesting behaviour; sociality is recorded for the first time within this bee genus. Analyses of provisioned nest cells and scopal pollen loads of females revealed that this species is polylectic (generalist), collecting pollen from plant species occurring in high abundance, namely Asteraceae, Zygophyllaceae and Oxalidaceae. The species is parasitized by the cuckoo bee Sphecodopsis semirufa (Cockerell), which is recorded for the first time to attack a halictid bee.
Patellapis/ sweat bee / biology / nest / communal / sociality / Halictidae
1. INTRODUCTION
The Namaqualand in western South Africa is renowned to be a “hotspot” of biodiver-sity (Myers et al., 2000) where plant-pollinator interactions are supposed to play a major role for coevolutionary processes and speci-ation (Johnson, 1996; Cowling et al., 1998; Johnson and Steiner, 2003). This region with its world wide unique overlap of plant and bee diversity centres (Kuhlmann, 2005) is char-acterised by an unusual selective regime of low, highly predictable rainfall, very rare pro-longed droughts, and mild, seasonal temper-ature ranges (Cowling et al., 1999) which is responsible for the species richness and the high degree of endemism in both plants and bees (Cowling and Hilton-Taylor, 1994). The Corresponding author: K. Timmermann,
ktimm_01@uni-muenster.de * Manuscript editor: Bryan Danforth
bee fauna of Namaqualand and its ecology is poorly investigated (Whitehead et al., 1987). This is especially true for the diverse halic-tid bee genus Patellapis Friese, which com-prises about 160 species, most of them con-fined to southern Africa and especially the South African winter rainfall area (Michener, 1978; Pauly, 1999). Species of this genus oc-cur in high abundance and they are assumed to play a major role as pollinators (Timmermann, 2005) but data on their biology is not available. Sweat bees (Halictidae) are of particular biological interest because of their diversity in social behaviour (Sakagami and Michener, 1962). Halictid social behaviour is charac-terised by the housing of a number of indi-viduals in the same nest, and, in some gen-era and subgengen-era, by a division of labour and castes (Lin, 1964). Halictid bees show a wide spectrum of social behaviour ranging from strictly solitary (brood rearing nests are each cared by a single female) to eusociality, with
Article published by EDP Sciences and available at http://www.apidologie.org
190 K. Timmermann, M. Kuhlmann
communal and semisocial life as presumed in-termediate forms (Sakagami, 1974; Richards, 1994). Because of their substantial intraspe-cific (Richards, 2000; Soucy and Danforth, 2002) and interspecific (Michener, 1974; Wcislo et al., 1993) variability in social be-haviour, halictid bees are ideal for researching social evolution and the evolutionary origins of sociality (Crespi, 1996; Danforth, 2002). Phylogenetic analyses have revealed that euso-ciality is of recent origin, evolving in three in-dependent lineages within the subfamily Hal-ictinae and including frequent reversals from eusociality to solitary nesting (Danforth, 1999, 2002; Danforth et al., 2003; Brady et al., 2006). In contrast, communal and semisocial nesting seems to have evolved independently from eusociality (Danforth, 2002). But hal-ictine social behaviour is not only extremely variable, but also ecologically and evolution-arily labile – reversals to solitary behavior seem to be quite common among the sweat bees (Richards, 1994). Due to geographic and climatic variation, some halictid species may even exhibit more than one type of sociality. Lasioglossum (Evylaeus) calceatum (Scopoli), for example, is social in lower alti-tudes but at higher altialti-tudes reverts to solitary behaviour (Sakagami and Munakata, 1972), and populations of Augochlorella striata (Po-vancher) in Nova Scotia showed, that many foundresses are unable to establish matrifilial societies in areas with short foraging sea-sons (Packer, 1990). Other examples of so-cially polymorphic halictines are Halictus
rubicundus (Christ) (Eickwort et al., 1996), Halictus sexcinctus (Fabricius) (Richards,
2001; Richards et al., 2003), and Lasioglossum
malachurum Kirby (Richards, 2000).
This paper provides the first information on the nesting biology and social organisation of a Patellapis species and gives strong sup-port for an additional case of independent evo-lution of sociality in halictid bees (Danforth, 2002). This is of particular interest because
Patellapis s.l. (sensu Michener, 2000)
repre-sents the most recent clade within the Halictini (Danforth et al., 2008) and is therefore of inter-est for understanding patterns of social evolu-tion.
The data presented here are based on obser-vations of a species new to science named P. sp. 1 here, which will be described in a forth-coming revision of Patellapis (Timmermann and Kuhlmann, unpubl. data).
2. MATERIALS AND METHODS 2.1. Study site
The study was carried out in the Nieuwoudtville Wild Flower Reserve (31◦21S 19◦08E; 760 m) in the South African winter rainfall area. Climat-ically, the Nieuwoudtville area is semi-arid with a mean annual rainfall of 341 mm (Snijman and Perry, 1987). The reserve falls within the vegetation type of the Nieuwoudtville dolerite renosterveld (Mucina and Rutherford, 2004) and is renowned for its high diversity of geophytes and annuals (Manning and Goldblatt, 1996).
2.2. Fieldwork
Fieldwork was conducted during the flowering seasons from August to October of 2002, 2004, and 2006. In each year, flower visiting individuals of P. sp. 1 were captured by using a sweep net dur-ing warm and sunny weather, mainly between 1100 and 1600 h, for the analyses of female scopal pollen loads. Observations on nesting individuals of P. sp. 1 were only made in 2006.
2.3. Nesting site
The gently sloping nesting site (5–10◦), covering an area of approximately 110 m2, was surrounded
Figure 1. (a) Nesting site of P. sp. 1 at the Nieuwoudtville Wild Flower Reserve, South Africa. (b) Nest entrance of P. sp. 1 (arrow). (c) Cuckoo bee Sphecodopsis semirufa. (d) Mating of P. sp. 1 on flower of Felicia australis (Asteraceae).
cicutarium (L.) L‘Hér (Geraniaceae), Spiloxene serrata (Thunb.) Garside (Hypoxidaceae), Bul-binella latifolia Kunth (Asphodelaceae), Cyanella hyacinthoides L. (Tecophilaeaceae), and Albuca maxima Burm.f. (Hyacinthaceae). The top soil layer, approximately 8–10 cm thick, consisted of very dry, hard and crusted substrate. Deeper, the soil gradually became moister and less condensed with a composition of 36% clay, 28% silt, and 36% sand. The soil-particle-size analysis followed the pipette-method of Köhn and Köttgen (Kretzschmar, 1989). The soil on the surface as well as below contained some small stones and a few roots.
2.4. Nest observation and excavation
Nest entrances were difficult to find because they tended to be hidden under low growing plants and they did not possess tumuli (Fig. 1b). We identi-fied nest entrances by observing the returning fe-males entering them. As a result of the hard soil, we excavated only a single nest, but observations on other six active nests were also made. For nest observations, the nest entrances were covered with clear plastic cups to count the number of adult fe-males within active nests. A single nest was
exca-vated in order to describe the architecture follow-ing the methodology of Sakagami and Michener (1962). The nest was filled with liquid latex which was allowed to harden. By this method it was possi-ble to follow the tunnels, to find brood cells and to reconstruct the architecture of the entire nest despite the very hard soil.
2.5. Pollen analyses
Host plants of P. sp. 1 were identified by analysing the content of female scopal pollen loads and larval food provisions of closed brood cells. The pollen was gently removed with an insect pin and embedded in Kaiser‘s glycerol gelatine on mi-croscope slides. Pollen samples were identified by light microscopy at a magnification of 400× with the help of a pollen reference collection represent-ing all plants flowerrepresent-ing at the study site. The pollen composition was investigated by identifying 400 pollen grains randomly chosen from each sample. The pollen grains representing less than 5% per load were assumed to be contamination and neglected (Westrich and Schmidt, 1986).
192 K. Timmermann, M. Kuhlmann
Figure 2. Nest of P. sp. 1. (a) Schematic represen-tation of the nest. (b) Same nest, top view. The dot represents the nest entrance. (c) Part of a branch with brood cells. (d) Side view of a closed and pro-visioned brood cell.
3. RESULTS
3.1. Nest architecture
The following information was obtained from excavating a single active nest on 6 September 2006. The nest contained eight adult females. The entrance was 3.5 mm in diameter and did not possess a tumulus. The main burrow entered the ground obliquely for the first centimetre, and then the burrow de-scended more or less vertically. Three lat-eral tunnels branched from the main burrow at depths of 15 cm, 18 cm, and 21 cm. Two of them divided again with some of the sec-ondary branches also ramified (Fig. 2a, b) to give eight laterals. Lateral tunnels extended 3–10 cm horizontally or slightly downward. The brood cells tended to be closely clustered along the branches (Fig. 2c). Eight to fifteen cells were clustered together and became more abundant towards the end of each branch. In total, 98 brood cells were observed for the whole nest, with 65 of them closed and 33 cells were open with unfinished larval food provi-sioning.
We made observations of P. sp. 1 on six other nests. The number of females belong-ing to a sbelong-ingle active nest varied from three to seven specimens (one nest with three, two nests with four, two nests with five females, and one nest with seven females).
3.2. Brood cells
The nest cells were elongated ovals, slightly flatter on the lower surface than on the up-per surface (Fig. 2d). All cells occurred in the moister substrate beneath the dry surface layer. They were found at depths of 17–27 cm with a maximum between 20–23 cm. The cells were primarily horizontal to subhorizontal in their orientation. In five of the cells the posterior end was slightly higher than the anterior end. Measurements of nine cells indicate an aver-age cell length from rear to centre of closure of 8.7 mm (range 8.3–9.6 mm) and an aver-age maximum width of 4.9 mm (range 4.6– 5.1 mm). The cell walls were completely lined with a thin and shiny waterproof film (tested with a droplet of water). Cell closures con-sisted of soil material not identical to the sur-rounding substrate and had an average width of 2.5 mm (range 2.2–3.0 mm). A vague spiral structure could be detected on the inner side of only one closure, the other eight were smooth. Closures were slightly concave on the inside and had no lining.
The provisions in closed cells were spheri-cal pollen-nectar balls of a pasty consistency with an average diameter of 4.2 mm (range 3.5–4.8 mm, n = 15). They were located on the bottom of the cells near the posterior end (Fig. 2d). Eggs were placed on the top of the provision with both ends attached to the masses (Fig. 2d). The whitish eggs were strongly arched and possessed a smooth, trans-parent chorion. Small to large sized larvae were also encountered but details of larval morphology and behaviour were not obtained.
3.3. Parasites
Figure 3. Seasonal activity pattern of P. sp. 1 (♀ black and♂ white bars) and its parasite Sphecodop-sis semirufa (♀ and ♂ dotted bars) at the Nieu-woudtville Wild Flower Reserve based on pooled records of the years 2002–2006 (P. sp. 1: n= 546, ♀ 292, ♂ 254; S. semirufa: n = 63, ♀ 47, ♂ 16). nesting site (Fig. 1c). Both species showed an overlapping daily and seasonal activity pattern (Fig. 3).
At the nesting site S. semirufa was seen patrolling around nests, performing inspection flights slowly and very close to the ground, and landing at several nests to inspect the entrances with their antennae. After inspection females usually flew onto a stick or plant close to the entrance and remained motionless (sometimes several minutes), observing the nest entrance. Several times the pollen loaded host bee was seen to arrive at the burrow and enter while the cuckoo bee was waiting. When P. sp. 1 left the nest, S. semirufa flew to the entrance, stopped in front of it, inspected the nest again with its antennae and then entered. We observed three females of S. semirufa invading a nest, stay-ing inside for three to eight minutes and leav-ing before the host female returned. Contact between the parasite and the host bee was not observed. Males of S. semirufa were regularly seen on flowers of F. australis, but no mating was observed.
3.4. Daily activity and seasonality
Females started flight activity on warm, clear or partly cloudy days at about 1115 h until 1700 h, but were most abundant from 1215 h to 1330 h. Periods of rainy and cloudy weather or incoming cold fronts disturbed bee activity, and the bees were not active outside nests. Females were seen particularly on
flow-ers of F. australis and Z. foetidum, which oc-curred in high abundance close to the nest-ing site. Males were regularly seen later in the day on host flowers near nests, where they pa-trolled or held territories. Mating was observed once on a flower of F. australis on 11 Septem-ber 2006 (Fig. 1d).
First observations at the nest aggregation were made on 27 August 2006, when nesting activities had already begun. When we last vis-ited the site on 27 September 2006, nesting ac-tivity was greatly reduced. Only a few females and almost no males visited the food plants, in-dicating that the nesting season was ending. A last single female of P. sp. 1 was collected on 19 October in the vicinity of the nesting site. Protandry is suggested by seasonal activity data of the males. Collection records indicate a single generation per year that is restricted to the winterly flowering season between August and October (Fig. 3).
3.5. Pollen analyses
From August to October 2006 we collected 223 specimens (♀ 198, ♂ 25) of Patellapis spec. at the Nieuwoudtville Wild Flower Re-serve. A total of 226 pollen samples were used for pollen analyses, including 161 samples from female scopal loads and 65 brood cells.
P. sp. 1 collected pollen from eight host plants
in seven plant families, including species of Asteraceae (F. australis, R. pumilum), Zy-gophyllaceae (Z. foetidum), Scrophulariaceae (Diascia spec.), Aizoaceae (G. sarcophylla), Oxalidaceae (O. pes-caprae), Asphodelaceae (B. latifolia) and Tecophilaeaceae (C.
hy-acinthoides) (Tab. I). Pollen from Asteraceae
194 K. Timmermann, M. Kuhlmann
Table I. Composition of 226 pollen samples of P. sp. 1 from the Nieuwoudtville Wild Flower Reserve 2006. Other= unidentified pollen types.
Family Host plant % (all loads) Presence in min.max./ load (%)
species samples
Asteraceae Felicia australis, 62.7 203 (89.8%) 6–100
Rhynchopsidium pumilum
Zygophyllaceae Zygophyllum foetidum 33.2 135 (59.7%) 6–100
Scrophulariaceae Diascia spec. 2.0 17 (7.5%) 6–100
Aizoaceae Galenia sarcophylla 1.5 12 (5.3%) 8–63
Oxalidaceae Oxalis pes-caprae 0.5 2 (0.9%) 30–75
Asphodelaceae Bulbinella latifolia < 0.1 2 (0.9%) 8–10 Tecophilaeaceae Cyanella hyacinthoides < 0.1 2 (0.9%) 8–15
Other < 0.1 1 (0.4%) 6
different plant families, most of them (n = 99) containing a mixture of Asteraceae and Zygo-phyllaceae.
Additional scopal pollen loads from 2002 (n = 12) were very similar in content, dominated by pollen of Asteraceae and Zygo-phyllaceae (together 85%). In 2004 the pollen content of scopal loads (n= 11) was very dif-ferent, consisting only of pollen from Oxali-daceae (76%) and Asteraceae (24%).
4. DISCUSSION
4.1. Sociality of the Patellapis species
Halictine bees are noteworthy among in-sects in the occurrence of different levels of social organization from strictly solitary to a complicated eusocial societies (Sakagami and Michener, 1962; Michener, 1974). Although, there is no strict correlation between social organisation and nest architecture (Sakagami and Michener, 1962), the communal sociality of P. sp. 1 seems to be very probable given the similarity in nest architectures of other communal halictid bees (Michener and Lange, 1958; Michener et al., 1979).
By definition, communality is the simplest form of insect social organisation (Paxton et al., 1996) where insects share a common nest in which each adult female provisions and produces its own offspring; there is a lack of reproductive division of labour and no overlap of generations (Michener, 1974). In such multi-female nests halictine bees tend
to have various degrees of integration of joint and solitary nest construction (Sakagami and Michener, 1962). The nest’s architecture is not an outcome of the work of a single bee, but a product of joint work by several nest mates. The joint and solitary sections in the nests are relatively easy to distinguish. The most dis-tinct pattern consists of one main communal burrow and several private laterals. Each in-habitant makes one or more laterals of their own (Sakagami and Michener, 1962). The P. spec. 1 multifemale nest appears to be com-munal. The ramifying nest suggests clear sep-aration of joint and solitary sections for repro-duction; eight adult females with equally worn wings and mandibles shared a single nest con-sisting of eight lateral tunnels with aggregated brood cells. Furthermore, several provisioned brood cells from different laterals suggest no collaboration of foragers in cell provisioning. It is assumed that each female had her own branch and own cells or cell group. A higher social organization of P. spec. 1 cannot be ex-cluded. However, eusociality is unlikely due to the single short activity period in winter.
some old brood cells within these nests. Both suggest, that one female simultaneously pro-vision more than one brood cell. Observations on nesting sites of P. spec. 1 have shown, that this species neither reuses old nests, nor seals the brood cells after egg deposition. Multiple provision of brood cells by a single female was not observed, but all open brood cells were completely empty. This might suggest some additional kinds of social interactions.
Although the nest architecture indicates a communal organisation for P. sp. 1, the level of social organisation is nevertheless not to-tally clear. Confirmation of communal status requires detailed studies of intranidal repro-ductive behaviour (Paxton et al., 1996), but such a study is lacking for the P. sp. 1. Evalu-ation of the reproductive status of individuals that share a nest can provide support for their communal status. A study of genetic related-ness and reproductive status of nestmates of P. sp. 1 is planned.
4.2. Cuckoo bee of the Patellapis species
The cleptoparasitic bee genus
Sphecodop-sis Bischoff comprises 10 species all endemic
to southern Africa (Eardley and Brothers, 1997; Michener, 2000). Among this genus only two host records are available. Rozen and Michener (1968) found eggs and larvae of Sphecodopsis capensis (Friese) in nests of Scrapter niger Lepeletier & Serville (as
Scrapter longula (Friese)) (Colletidae) and Sphecodopsis fumipennis Bischoff in those
of Scrapter erubescens (Friese) (as Scrapter
crassula Cockerell). Their flight and
in-spection behaviour described in Rozen and Michener (1968) is identical with that of
Sphe-codopsis semirufa observed at nests of P.
sp. 1. Sphecodopsis has not previously been recorded kleptoparasitizing halictine bees.
S. semirufa probably has more than one host
species, because it is distributed throughout the Karoo area (Eardley and Brothers, 1997), where P. sp. 1 has not been recorded.
4.3. Polylecty of Patellapis sp. 1
There is great diversity among bees in their patterns of pollen use, with a continuum
from generalists that use pollen from many plant taxa of different families to specialists that collect pollen from just one plant species (Linsley, 1958; Cane and Sipes, 2006). Anal-yses of pollen collected by P. sp. 1 females showed that these bees are polylectic accord-ing to the definition of Cane and Sipes (2006) with strong preferences for plant species oc-curring in high abundance. In 2002 and 2006
F. australis, R. pumilum and Z. foetidum were
the most abundant flowers at the nesting site and the preferred pollen plants of P. sp. 1. In 2004 Oxalis pes-caprae and O. obtusa were exceptionally abundant and the most impor-tant host plants. Flower visiting records by Gess and Gess (2004) support a relatively high incidence of polylecty in South African halictine bees with a strong preference for Asteraceae and Zygophyllaceae. Oxalidaceae as host plants for halictids are recorded here for the first time.
ACKNOWLEDGEMENTS
The work was funded in part by the German Academic Exchange Service (DAAD) to the first author. We would like to thank the Northern Cape Nature Conservation for permission to work in the Nieuwoudtville Wild Flower Reserve. Furthermore, we thank Lillian Harris for improving the language. The manuscript was greatly improved by the com-ments of Bryan N. Danforth and three anonymous reviewers.
Biologie de l’espèce Patellapis (s.str., Hymenop-tera : Apoidea : Halictidae) : première descrip-tion d’un comportement social chez ce genre d’abeilles.
Halictidae/ abeille / biologie / socialité / nidifica-tion/ nid collectif
Zusammenfassung – Biologie einer
Patella-pis-Art (s.str., Hymenoptera: Apoidea:
196 K. Timmermann, M. Kuhlmann
Saisonalität und identifizierten den Kleptoparasi-ten einer neuen Art von Patellapis (s. str.), die wir vorläufig als P. sp. 1 bezeichneten. Eine kleine Nestaggregation dieser Art wurde in der Nä-he von Nieuwoudtville (31◦21S 19◦08E; 760 m) (Abb. 1a, c) untersucht. Adulte Bienen flogen hier in der Umgebung des Nestbereiches von August bis Oktober 2006 (Abb. 3). Die Nesteingänge von P. sp. 1 waren nicht leicht zu finden, da sie meist unter bodennahen Pflanzen versteckt waren und keine Tu-muli besaßen (Abb. 1b). Mehrere Weibchen wurden beobachtet, wie sie denselben Nesteingang benutz-ten. Dies lässt auf soziales Verhalten schließen. Um Nester beobachten zu können, wurden 7 Nestein-gänge mit durchsichtigen Plastikbechern bedeckt und so die Anzahl der adulten Weibchen in diesen aktiven Nestern gezählt. Die Anzahl an Weibchen pro Nest reichte von drei bis acht. Wegen des harten Bodens gruben wir nur ein einziges Nest aus, um die Nestarchitektur zu beschreiben. Das Nest be-steht aus einem einzigen Hauptgang mit mehreren seitlichen Tunneln (Abb. 2a). Insgesamt wurden 98 Zellen im Nest in einer Tiefe von 17–27 cm gefun-den (Abb. 2c, d). Unsere Beobachtungen sowie die Nestarchitektur, die sehr ähnlich ist wie bei anderen kommunalen Halictiden, weisen darauf hin, dass P. sp. 1 kommunal nistet (die einfachste Form der so-zialen Organisation bei Insekten). Dies ist die erste Beschreibung einer kommunalen Nestorganisation innerhalb der Gattung Patellapis. Dies lässt auf eine unabhängige Evolution des Sozialverhaltens in der Gattung Patellapis schließen. Bei den Pollenvorrä-ten der Brutzellen sowie zusätzlich an 161 Pollen-ladungen von den Scopalhaaren der Weibchen wur-den Pollenanalysen durchgeführt. Dabei zeigte sich, dass diese Bienenart ein Generalist (polylektisch) ist mit einem starken Übergewicht an Pflanzenar-ten aus den Gruppen der Asteraceae, Zygophylla-ceae und OxalidaZygophylla-ceae (Tab. I). Die Kuckucksbiene Sphecodopsis semirufa (Cockerell) wurde als Klep-toparasit von P. sp. 1 bestimmt (Abb. 1c). Bisher wurde noch nie beobachtet, dass Sphecodopsis bei Halictiden parasitiert.
Patellapis / Furchenbienen / Biologie / Nest /
kommunal/ Sozialität / Halictidae
REFERENCES
Brady S.G., Sipes S., Pearson A., Danforth B.N. (2006) Recent and simultaneous origins of euso-ciality in halictid bees, Proc. R. Soc. Lond. B Biol. Sci. 273, 1643–1649.
Cane J.H., Sipes S. (2006) Characterizing floral spe-cialization by bees: analytical methods and a re-vised lexicon for oligolecty, in: Waser M., Ollerton J. (Eds.), Plant-Pollinator interactions, From spe-cialization to generalization, The University of Chicago Press, Chicago and London, pp. 99–122.
Cowling R.M., Hilton-Taylor C. (1994) Patterns of plant diversity and endemism in southern Africa: an overview, Strelitzia 1, 31–52.
Cowling R.M., Rundel P.W., Desmet P.G., Esler K.J. (1998) Extraordinary high regional-scale plant di-versity in southern African arid lands: subconti-nental and global comparisons, Divers. Distrib. 4, 27–36.
Cowling R.M., Esler K.J., Rundel P.W. (1999) Namaqualand, South Africa – an overview of a unique winter-rainfall desert ecosystem, Plant Ecol. 142, 3–21.
Crespi B.J. (1996) Comparative analysis of the ori-gins and losses of eusociality: causal mosaics and historical uniqueness, in: Martins E.P. (Ed.), Phylogenies and the comparative method in ani-mal behaviour, Oxford University Press, Oxford, pp. 253–287.
Danforth B.N. (1999) Phylogeny of the bee genus Lasioglossum (Hymenoptera: Halictidae) based on mitochondrial COI sequence data, Syst. Entomol. 24, 377–393.
Danforth B.N. (2002) Evolution of sociality in a prim-itively eusocial lineage of bees, Proc. Natl. Acad. Sci. (USA) 99, 286–290.
Danforth B.N., Conway L., Ji S. (2003) Phylogeny of eusocial Lasioglossum reveals multiple losses of eusociality within a primitively eusocial clade of bees (Hymenoptera: Halictidae), Syst. Biol. 52, 23–35.
Danforth B.N., Eardley C., Packer L., Walker K., Pauly A., Randrianambinintsoa F. (2008) Phylogeny of Halictidae with an emphasis on endemic African Halictinae, Apidologie 39, 86–101.
Eardley C.D., Brothers D.J. (1997) Phylogeny of the Ammobatini and revision of the Afrotropical gen-era, J. Hym. Res. 6, 353–418.
Eickwort G.C., Eickwort J.M., Gordon J., Eickwort M.A. (1996) Solitary behaviour in a high-altitude population of the social sweat bee Halictus rubi-cundus (Hymenoptera: Halictidae), Behav. Ecol. Sociobiol. 38, 227–233.
Gess S.K., Gess F.W.(2004) A comparative overview of flower visiting by non-Apis bees in the semi-arid to semi-arid areas of Southern Africa, J. Kans. Entomol. Soc. 77, 602–618.
Johnson S.D. (1996) Pollination, adaptation and spe-ciation models in the Cape flora of South Africa, Taxon 45, 59–66.
Johnson S.D., Steiner K.E. (2003) Specialized pollina-tion systems in southern Africa, S. Afr. J. Sci. 99, 345–348.
Kerfoot W.B. (1967) Nest architecture and associated behavior of the nocturnal bee Sphecodogastra tex-ana (Hymenoptera: Halictidae), J. Kans. Entomol. Soc. 40, 84–93.
Kuhlmann M. (2005) Diversity, distribution pat-terns and endemism of southern African bees (Hymenoptera: Apoidea), in: Huber B.A., Sinclair B.J., Lampe K.-H. (Eds.), African biodiversity: Molecules, organisms, ecosystems, Proc. 5th Int. Symp. on Tropical Biology, Museum König, Springer Verlag, Bonn, pp. 167–172.
Lin N. (1964) Increased parasitic pressure as a major factor in the evolution of social behaviour in hal-ictine bees, Insectes Soc. 11, 187–192.
Linsley E.G. (1958) The ecology of solitary bees, Hilgardia 27, 543–599.
Manning J.C., Goldblatt P. (1996) The Prosoeca peringuyei (Diptera: Nemestrinidae) pollination guild in southern Africa: long-tongued flies and their tubular flowers, Ann. Mo. Bot. Gard. 83, 67– 86.
Michener C.D. (1974) The social behaviour of the bees. A comparative study, Belknap Press of Harvard University Press, Cambridge, MA. Michener C.D. (1978) The classification of halictine
bees: tribes and Old World nonparasitic genera with strong venation, Univ. Kansas Sci. Bull. 51, 501–538.
Michener C.D. (2000) The bees of the world, The Johns Hopkins Press, Baltimore.
Michener C.D., Lange R.B. (1958) Observations on the behaviour of Brazilian halictid bees (Hymenoptera, Apoidea), I, Pseudagapostemon, Ann. Entom. Soc. Am. 51, 154–164.
Michener C.D., Breed M.D., Bell W.J. (1979) Seasonal cycles, nests, and social behaviour of some Colombian halictine bees (Hymenoptera; Apoidea), Rev. Biol. Trop. 27, 13–34.
Mucina L., Rutherford M.C. (2004) Vegetation map of South Africa, Lesotho and Swaziland, National Botanical Institute, Pretoria.
Myers N., Mittermeier R.A., Mittermeier C.G., da Fonseca G.A.B., Kent J. (2000) Biodiversity hotspots for conservation priorities, Nature 403, 853–858.
Packer L. (1990) Solitary and eusocial nests in a population of Augochlorella striata (Provancher) (Hymenoptera; Halictidae) at the northern edge of its range, Behav. Ecol. Sociobiol. 27, 339–344. Pauly A. (1999) Classification des Halictini de
la région Afrotropicale (Hymenoptera, Apoidea, Halictidae), Bull. Inst. R. Sci. Nat. Belg. Entomol. 69, 137–196.
Paxton R.J., Thorén P.A., Tengö J., Estoup A., Pamilo P. (1996) Mating structure and nestmate re-latedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatel-lites, Mol. Ecol. 5, 511–519.
Richards M.H. (1994) Social evolution in the genus Halictus: a phylogenetic approach, Insectes Soc. 41, 315–325.
Richards M.H. (2000) Evidence for geographic vari-ation in colony social organizvari-ation of an obli-gately social sweat bee, Lasioglossum malachu-rum Kirby (Hymenoptera; Halictidae), Can. J. Zool. 78, 1259–1266.
Richards M.H. (2001) Nesting biology and social or-ganization of Halictus sexcinctus (Fabricius) in southern Greece, Can. J. Zool. 79, 2210–2220. Richards M.H., von Wettberg E.J., Rütgers A.C.
(2003) A novel social polymorphism in a primi-tively eusocial bee, Proc. Natl. Acad. Sci. (USA) 100, 7175–7180.
Rozen J.G., Michener C.D. (1968) The biology of Scrapter and its cuckoo bee, Pseudodichroa (Hymenoptera: Colletidae and Anthophoridae), Am. Mus. Novit. 2335, 1–13.
Sakagami S.F. (1974) Sozialstruktur und Polymorphis-mus bei Furchen- und Schmalbienen (Halictinae), in: Schmidt G.H. (Ed.), Sozialpolymorphismus bei Insekten. Probleme der Kastenbildung im Tierreich, Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp. 257–293.
Sakagami S.F., Michener C.D. (1962) The nest archi-tecture of the sweat bees (Halictinae) – a compara-tive study of behaviour, The University of Kansas Press, Lawrence.
Sakagami S.F., Munakata M. (1972) Distribution and bionomics of a transpaleartic eusocial halictine bee, Lasioglossum (Evylaeus) calceatum, in north-ern Japan, with reference to its solitary life cycle at high altitude, J. Fac. Sci. Hokkaido Univ. Ser. 6 (Zool.) 18, 411–439.
Snijman D., Perry P. (1987) A floristic analysis of the Nieuwoudtville Wild Flower Reserve, north-western Cape, S. Afr. J. Bot. 53, 445–454. Soucy S.L., Danforth B.N. (2002) Phylogeography of
the socially polymorphic sweat bee Halictus rubi-cundus (Hymenoptera: Halictidae), Evolution 56, 330–341.
Timmermann K. (2005) Bee communities (Hymenoptera: Apoidea) of different vegeta-tion types in the semiarid part of western South Africa – structure and pollen specialisation (in German), Masters thesis (unpubl.), University of Münster.
Wcislo W.T., Wille A., Orozco E. (1993) Nesting biology of tropical solitary and social sweat bees, Lasioglossum (Dialictus) figueresi Wcislo and Lasioglossum (D.) aeneiventre (Friese) (Hymenoptera: Halictidae), Insectes Soc. 40, 21–40.
Westrich P., Schmidt K. (1986) Methoden und Anwendungsgebiete der Pollenanalyse bei Wildbienen (Hymenoptera, Apoidea), Linz. Biol. Beitr. 18, 341–360.
